Crossref journal-article
Rockefeller University Press
The Journal of Cell Biology (291)
Abstract

Muscle cells are frequently subjected to severe conditions caused by heat, oxidative, and mechanical stresses. The small heat shock proteins (sHSPs) such as αB-crystallin and HSP27, which are highly expressed in muscle cells, have been suggested to play roles in maintaining myofibrillar integrity against such stresses. Here, we identified a novel member of the sHSP family that associates specifically with myotonic dystrophy protein kinase (DMPK). This DMPK-binding protein, MKBP, shows a unique nature compared with other known sHSPs: (a) In muscle cytosol, MKBP exists as an oligomeric complex separate from the complex formed by αB-crystallin and HSP27. (b) The expression of MKBP is not induced by heat shock, although it shows the characteristic early response of redistribution to the insoluble fraction like other sHSPs. Immunohistochemical analysis of skeletal muscle cells shows that MKBP localizes to the cross sections of individual myofibrils at the Z-membrane as well as the neuromuscular junction, where DMPK has been suggested to be concentrated. In vitro, MKBP enhances the kinase activity of DMPK and protects it from heat-induced inactivation. These results suggest that MKBP constitutes a novel stress-responsive system independent of other known sHSPs in muscle cells and that DMPK may be involved in this system by being activated by MKBP. Importantly, since the amount of MKBP protein, but not that of other sHSP family member proteins, is selectively upregulated in skeletal muscle from DM patients, an interaction between DMPK and MKBP may be involved in the pathogenesis of DM.

Bibliography

Suzuki, A., Sugiyama, Y., Hayashi, Y., Nyu-i, N., Yoshida, M., Nonaka, I., Ishiura, S., Arahata, K., & Ohno, S. (1998). MKBP, a Novel Member of the Small Heat Shock Protein Family, Binds and Activates the Myotonic Dystrophy Protein Kinase. The Journal of Cell Biology, 140(5), 1113–1124.

Authors 9
  1. Atsushi Suzuki (first)
  2. Yuki Sugiyama (additional)
  3. Yukiko Hayashi (additional)
  4. Nobuo Nyu-i (additional)
  5. Michihiko Yoshida (additional)
  6. Ikuya Nonaka (additional)
  7. Sho-ichi Ishiura (additional)
  8. Kiichi Arahata (additional)
  9. Shigeo Ohno (additional)
References 48 Referenced 116
  1. 10.1093/oxfordjournals.jbchem.a123665 / J Biochem / αB-crystallin in skeletal muscle: purification and localization by Atomi (1991)
  2. 10.1161/01.RES.71.2.288 / Circ Res / αB-crystallin cardiac tissue. Association with actin and desmin filaments by Bennardini (1992)
  3. 10.1016/S0925-4439(96)00057-9 / Biochim Biophys Acta / Normal levels of DM RNA and myotonin protein kinase in skeletal muscle from adult myotonic dystrophy (DM) patients by Bhagwati (1996)
  4. 10.1016/0092-8674(92)90154-5 / Cell / Molecular basis of myotonic dystrophy: expansion of a trinucleotide (CTG) repeat at the 3′ end of a transcript encoding a protein kinase family member by Brook (1992)
  5. 10.1152/ajplegacy.1971.221.2.427 / Am J Physiol / Tissue temperatures and whole-animal oxygen consumption after exercise by Brooks (1971)
  6. 10.1152/ajplegacy.1971.220.4.1053 / Am J Physiol / Temperature, skeletal muscle mitochondrial functions, and oxygen debt by Brooks (1971)
  7. 10.1007/BF00163229 / J Mol Evol / The expanding small heat-shock protein family, and structure predictions of the conserved “α-crystallin domain” by Caspers (1995)
  8. 10.1073/pnas.94.14.7388 / Proc Natl Acad Sci USA / Expansion of a CUG trinucleotide repeat in the 3′ untranslated region of myotonic dystrophy protein kinase transcripts results in nuclear retention of transcripts by Davis (1997)
  9. 10.1016/S0006-291X(82)80124-1 / Biochem Biophys Res Commun / Free radicals and tissue damage produced by exercise by Davis (1982)
  10. 10.1021/bi00201a031 / Biochemistry / Phosphorylation reactions of recombinant human myotonic dystrophy protein kinase and their inhibition by Dunne (1994)
  11. 10.1007/BF03348900 / J Endocrinol Invest / Muscle autoantigens in thyroid associated ophthalmopathy: the limits of molecular genetics by Elisei (1993)
  12. 10.1126/science.1546326 / Science / An unstable triplet repeat in a gene related to myotonic muscular dystrophy by Fu (1992)
  13. 10.1126/science.8469976 / Science / Decreased expression of myotonin-protein kinase messenger RNA and protein in adult form of myotonic dystrophy by Fu (1993)
  14. 10.1073/pnas.94.14.7394 / Proc Natl Acad Sci USA / Transcriptional abnormality in myotonic dystrophy affects DMPK but not neighboring genes by Hamshere (1997)
  15. {'key': '2023072207410234200_B15'}
  16. 10.1016/0022-510X(93)90191-Z / J Neurol Sci / Abnormal localization of laminin subunits in muscular dystrophies by Hayashi (1993)
  17. 10.1002/jcp.1041590107 / J Cell Physiol / Coordinate and independent regulation of αB-crystallin and HSP27 expression in response to physiological stress by Head (1994)
  18. 10.1021/bi00536a008 / Biochemistry / Modulation of heat-shock polypeptide synthesis in HeLa cells during hyperthermia and recovery by Hickey (1982)
  19. 10.1073/pnas.79.7.2360 / Proc Natl Acad Sci USA / Four small Drosophila heat shock proteins are related to each other and to mammalian α-crystallin by Ingolia (1982)
  20. 10.1083/jcb.125.6.1385 / J Cell Biol / Sense and antisense modification of glial αB-crystallin production results in alterations of stress fiber formation and thermoresistance by Iwaki (1994)
  21. 10.1006/geno.1997.4956 / Genomics / Identification and characterization of the gene encoding a new member of the α-crystallin/small hsp family, closely linked to the αB-crystallin gene in a head-to-head manner by Iwaki (1997)
  22. 10.1016/S0021-9258(18)53882-5 / J Biol Chem / Small heat shock proteins are molecular chaperones by Jakob (1993)
  23. 10.1074/jbc.271.25.15187 / J Biol Chem / Investigation of myotonic dystrophy kinase isoform translocation and membrane association by James (1996)
  24. 10.1038/ng0792-261 / Nat Genet / Characterization of the myotonic dystrophy region predicts multiple protein isoform- encoding mRNAs by Jansen (1992)
  25. 10.1038/ng0796-316 / Nat Genet / Abnormal myotonic dystrophy protein kinase levels produce only mild myopathy in mice by Jansen (1996)
  26. 10.1016/S0021-9258(18)42574-4 / J Biol Chem / Copurification of small heat shock protein with αB-crystallin from human skeletal muscle by Kato (1992)
  27. 10.1016/S0021-9258(17)36606-1 / J Biol Chem / Purification and characterization of a 20-kD protein that is highly homologous to αB-crystallin by Kato (1994)
  28. 10.1073/pnas.88.9.3652 / Proc Natl Acad Sci USA / αB-crystallin is a small heat shock protein by Klemenz (1991)
  29. 10.1016/S0014-5793(97)00541-3 / FEBS Lett / Activation of protein kinase B (Akt/RAC-protein kinase) by cellular stress and its association with heat shock protein Hsp27 by Konishi (1997)
  30. 10.1016/S0021-9258(18)53711-X / J Biol Chem / Induction of Chinese hamster HSP27 gene expression in mouse cells confers resistance to heat shock by Lavoie (1993)
  31. 10.1016/S0021-9258(20)80512-2 / J Biol Chem / Modulation of actin microfilament dynamics and fluid phase pinocytosis by phosphorylation of heat shock protein 27 by Lavoie (1993)
  32. 10.1128/MCB.15.1.505 / Mol Cell Biol / Modulation of cellular thermoresistance and actin filament stability accompanies phosphorylation-induced changes in the oligomeric structure of heat shock protein 27 by Lavoie (1995)
  33. 10.1146/annurev.ge.22.120188.003215 / Annu Rev Genet / The heat shock proteins by Linquist (1988)
  34. 10.1074/jbc.270.35.20246 / J Biol Chem / Identification, tissue-specific expression, and subcellular localization of the 80 and 71kD forms of myotonic dystrophy kinase protein by Maeda (1995)
  35. 10.1126/science.1546325 / Science / Myotonic dystrophy mutation: an unstable CTG repeat in the 3′ untranslated region of the gene by Mahadevan (1992)
  36. 10.4049/jimmunol.154.1.363 / J Immunol / Constitutive expression of human hsp27, Drosophila hsp27, or human αB-crystallin confers resistance to TNF- and oxidative stress-induced cytotoxicity in stably transfected murine L929 fibroblasts by Mehlen (1995)
  37. 10.1083/jcb.114.2.255 / J Cell Biol / A 25-kD inhibitor of actin polymerization is a low molecular mass heat shock protein by Miron (1991)
  38. 10.1006/bbrc.1997.6706 / Biochem Biophys Res Commun / Angiotensin II is not necessary for stretch-induced MAP kinase activation in cardiomyocytes by Nyui (1997)
  39. 10.1126/science.274.5293.1613 / Science / Expanding the eukaryote's cast of chaperones by Pennisi (1996)
  40. 10.1016/S0021-9258(17)36828-X / J Biol Chem / Chaperone-like activity of α-crystallin by Rao (1994)
  41. 10.1038/ng0796-325 / Nat Genet / Mice lacking the myotonic dystrophy protein kinase develop a late onset progressive myopathy by Reddy (1996)
  42. 10.1016/0092-8674(94)90003-5 / Cell / Protein folding and the regulation of signaling pathways by Rutherford (1994)
  43. 10.1038/ng0793-233 / Nat Genet / Effect of the myotonic dystrophy (DM) mutation on mRNA levels of the DM gene by Sabouri (1993)
  44. 10.1016/0014-5793(94)00808-6 / FEBS Lett / Expression of a novel human myotonin protein kinase (MtPK) cDNA clone which encodes a protein with a thymopoietin-like domain in COS cells by Sasagawa (1994)
  45. 10.1083/jcb.128.3.373 / J Cell Biol / Mammalian α1- and β1-syntrophin bind to the alternative splice-prone region of the dystrophin COOH terminus by Suzuki (1995)
  46. 10.1083/jcb.128.6.995 / J Cell Biol / Foci of trinucleotide repeat transcripts in nuclei of myotonic dystrophy cells and tissues by Taneja (1995)
  47. 10.1093/hmg/4.4.599 / Hum Mol Genet / Myotonic dystrophy: evidence for a possible dominant-negative RNA mutation by Wang (1995)
  48. 10.1093/hmg/4.6.1063 / Hum Mol Genet / Characterization of myotonin dystrophy kinase (DMK) protein in human and rodent muscle and central nervous tissue by Whiting (1995)
Dates
Type When
Created 23 years, 1 month ago (July 26, 2002, 12:47 p.m.)
Deposited 2 years, 1 month ago (July 22, 2023, 3:42 a.m.)
Indexed 2 months, 1 week ago (June 19, 2025, 5:01 p.m.)
Issued 27 years, 5 months ago (March 9, 1998)
Published 27 years, 5 months ago (March 9, 1998)
Published Online 27 years, 5 months ago (March 9, 1998)
Published Print 27 years, 5 months ago (March 9, 1998)
Funders 0

None

@article{Suzuki_1998, title={MKBP, a Novel Member of the Small Heat Shock Protein Family, Binds and Activates the Myotonic Dystrophy Protein Kinase}, volume={140}, ISSN={1540-8140}, url={http://dx.doi.org/10.1083/jcb.140.5.1113}, DOI={10.1083/jcb.140.5.1113}, number={5}, journal={The Journal of Cell Biology}, publisher={Rockefeller University Press}, author={Suzuki, Atsushi and Sugiyama, Yuki and Hayashi, Yukiko and Nyu-i, Nobuo and Yoshida, Michihiko and Nonaka, Ikuya and Ishiura, Sho-ichi and Arahata, Kiichi and Ohno, Shigeo}, year={1998}, month=mar, pages={1113–1124} }